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Evolutionary Dynamics of Host Specialization in Wood-Decay Fungi

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Evolutionary Dynamics of Host Specialization in Wood-Decay Fungi Krah et al. BMC Evolutionary Biology (2018) 18:119 https://doi.org/10.1186/s12862-018-1229-7 RESEARCHARTICLE Open Access Evolutionary dynamics of host specialization in wood-decay fungi Franz-Sebastian Krah1,2* , Claus Bässler2, Christoph Heibl2, John Soghigian3, Hanno Schaefer1 and David S. Hibbett4 Abstract Background: The majority of wood decomposing fungi are mushroom-forming Agaricomycetes, which exhibit two main modes of plant cell wall decomposition: white rot, in which all plant cell wall components are degraded, including lignin, and brown rot, in which lignin is modified but not appreciably removed. Previous studies suggested that brown rot fungi tend to be specialists of gymnosperm hosts and that brown rot promotes gymnosperm specialization. However, these hypotheses were based on analyses of limited datasets of Agaricomycetes. Overcoming this limitation, we used a phylogeny with 1157 species integrating available sequences, assembled decay mode characters from the literature, and coded host specialization using the newly developed R package, rusda. Results: We found that most brown rot fungi are generalists or gymnosperm specialists, whereas most white rot fungi are angiosperm specialists. A six-state model of the evolution of host specialization revealed high transition rates between generalism and specialization in both decay modes. However, while white rot lineages switched most frequently to angiosperm specialists, brown rot lineages switched most frequently to generalism. A time- calibrated phylogeny revealed that Agaricomycetes is older than the flowering plants but many of the large clades originated after the diversification of the angiosperms in the Cretaceous. Conclusions: Our results challenge the current view that brown rot fungi are primarily gymnosperm specialists and reveal intensive white rot specialization to angiosperm hosts. We thus suggest that brown rot associated convergent loss of lignocellulose degrading enzymes was correlated with host generalism, rather than gymnosperm specialism. A likelihood model of host specialization evolution together with a time-calibrated phylogeny further suggests that the rise of the angiosperms opened a new mega-niche for wood-decay fungi, which was exploited particularly well by white rot lineages. Keywords: Wood-decay fungi, Decay mode, White rot, Brown rot, Host specialization, R package rusda Background chains of glucose subunits that can take on a recalcitrant About 2000 billion tons of carbon is present in terres- crystalline form [6]. Hemicelluloses are matrix polysac- trial ecosystems [1], of which 550 billion tons are fixed charides consisting of various heteropolymers, e.g., of in vegetation [2]. In forest ecosystems, most plant bio- xylans and glucomannans [7]. Lignin is a complex aro- mass is stored in the form of dead wood [3]. Woody matic polymer that is resistant to hydrolytic degradation plant cell walls consist mainly of the lignocellulose com- [8]. The amount of cellulose in woody plants is 40–50% plex which is composed of the polymeric polysaccha- of the wood dry weight and for hemicelluloses and lignin rides cellulose, hemicellulose and lignin heteropolymers 15–30% each. The plant biomass further consists of [4, 5]. Cellulose is a macropolymer consisting of linear macromolecules such as lipids, waxes, proteins and phenolic compounds [3]. The most efficient agents of * Correspondence: [email protected] the decay of the lignocellulose complex are saprotrophic 1Plant Biodiversity Research Group, Center for Food and Life Sciences fungi, which therefore play pivotal roles in the cycling of Weihenstephan, Technische Universität München, Freising, Germany 2Baverian Forest National Park, Grafenau, Germany carbon [9] and nutrients [10] in the forest ecosystem. Full list of author information is available at the end of the article Wood is produced by angiosperms and gymnosperms, © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Krah et al. BMC Evolutionary Biology (2018) 18:119 Page 2 of 13 which together comprise more than 60,000 species [11]. are distinguished by high copy numbers of genes encod- Angiosperms regularly have lower amounts of lignin ing different carbohydrate-active enzymes (CAZymes) than gymnosperms, whereas angiosperms regularly have which are classified based on the CAZy database [27]. In higher amounts of cellulose than gymnosperms [12, 13]. general, CAZymes, which act on crystalline cellulose are Further, angiosperms often have lower amounts of more abundant in white rot genomes compared with non-structural secondary compounds (plant extractives) brown rot [24]. Glycoside hydrolase (GH) families (e.g., than gymnosperms [12–15], with some exceptions, e.g., GH6 and GH7, including cellobiohydrolases) are more species of the genera Quercus, Fagus or Malus [16]. abundant in white rot compared with brown rot fungi The main agents of wood decay are members of the [24]. Further, lytic polysaccharide monooxygenases class Agaricomycetes (Basidiomycota). Agaricomycetes (LPMOs) from the AA9 family are more abundant in contains about 21,000 species with a worldwide distribu- white than brown rot fungi [24]. Apart from Agaricomy- tion, including many lifestyles, e.g. mycorrhizal symbi- cetes, LPMOs can be found in Ascomycetes and Mucor- onts, pathogens, and saprotrophs. Most saprotroph omycotina [21, 24]. Finally, lignin-degrading class II fungi within the Agaricomycetes are dead wood decaying peroxidases (AA2) and other heme-containing peroxi- fungi. Dead wood decay modes can be classified as ei- dases are more common in white rot, and reduced or ther white or brown rot. Brown rot fungi attack cellulose absent in brown rot fungi [26] (for mechanisms of action but do not significantly degrade lignin [17], resulting in see Hofrichter et al. [28]). The most recent common an- a brownish residue that breaks into cubical fragments, cestor of Agaricomycetes was a white rot species (based whereas white rot fungi degrade both cellulose and lig- on an inferred expansions of AA2 and other lignocellu- nin [18], leaving a bleached fibrous residue (Fig. 1). lolytic enzymes) with at least four independent origins of Hemicellulose can be degraded by both brown and white brown rot, correlated with parallel losses of genes en- rot fungi [19]. Whereas dead wood is mainly decayed by coding diverse CAZys, and the complete loss of lignino- Agaricomycetes, in plant litter decay, Ascomycota play a lytic class II peroxidases (AA2) [24], making reversals to significant role along with litter-decomposing Agarico- white rot unlikely. This white rot ancestor likely lived mycetes [19, 20]. Other decay modes are also present, roughly 290 (+/− ca. 70) million years ago (MYA) [24]. such as “soft rot” in some Ascomycota and “grey rot” in Analyses of a sample of 62 genomes by Nagy et al. [29] some Basidiomycota such as Schizophyllum commune suggested that expansions of cellobiohydrolases (GH6, [21]. Although many ectomycorrhizal fungi are partially GH7), LPMOs (AA9), and other plant cell wall degrad- saprotrophic, their decay abilities are considered mar- ing enzymes occurred early in the evolution of Agarico- ginal compared to wood decay fungi [22, 23]. mycetes, prior to the expansion of class II peroxidases The enzymatic basis of the differences between white (AA2). rot and brown rot has been studied extensively in com- Gilbertson [30] investigated ecological differences be- parative genomic analyses [21, 24–26]. White rot fungi tween white and brown rot decay modes, noting that a c b d Fig. 1 Brown and white rot residues and fungal fruit bodies. a) Brown rot residue, b) brown rot fungus, Fomitopsis pinicola (Polyporales, Fomitopsidaceae), c) white rot residue, d) white rot fungus, Fomes fomentarius (Polyporales, Polyporaceae). Photos by F.-S. Krah (a,b,c) and Heinrich Holzer (d) Krah et al. BMC Evolutionary Biology (2018) 18:119 Page 3 of 13 brown rot fungi preferentially occur on gymnosperm interpretations, we re-sampled a single species per genus hosts [31]. Gilbertson thus suggested a correlated evolu- from our final dataset (hereafter “one-genus-subset”)and tion of brown rot decay mode and gymnosperm repeated the analyses described below 100 times. specialization. Hibbett and Donoghue [32] tested Gil- To gather data on host associations, we used the R bertson’s hypothesis using phylogenetic comparative package “rusda”, written for this study, as an interface to methods. Their results suggested that the evolution of the USDA Fungus-Host Distribution Database (FHDD) brown rot was correlated with the evolution of exclusive [33]. The FHDD contains fungus-host combinations, but decay of gymnosperm hosts. However, this inference was does not provide information on the occurrence fre- made from a dataset with limited taxonomic sampling, quencies on a particular host (other than the number of with only a total of 130 species [32]. published records on each host). The “rusda” package To assess the evolution of decay modes and
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